Involvement of Selenium in Regulating Plant Ecosystems

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1		Feng Xu	--	2336	2022-10-25 05:48:51

This entry is adapted from the peer-reviewed paper 10.3390/plants11202712

Selenium is an essential trace mineral nutrient for humans and animals and has important functions in enhancing immunity, scavenging free radicals in the body, and preventing cardiovascular diseases. Selenium deficiency poses a great risk to human health, triggering macrosomia, immune deficiency, impaired fertility, Keshan disease, and Kashin–Beck disease. However, excessive Se intake also causes selenosis, the main symptoms of which are respiratory distress, vomiting, abdominal pain, and diarrhea. Selenium is widely but heterogeneously distributed in the natural environment, and soil total Se content is significantly correlated with the soil parent material and climatic conditions. The average total Se content of soil around the world ranges from 0.1 mg·kg⁻¹ to 2.0 mg·kg⁻¹, and the median concentration in Chinese soils is 0.219 mg·kg⁻¹. In the typically Se-rich areas in Enshi Tujia and Miao Autonomous Prefecture, Hubei Province, the Se content in the topsoil is 0.84 ± 1.39 mg·kg⁻¹. Soil Se deficiency zones are widespread across the globe, and currently approximately 0.5–1.0 billion people are at risk of Se deficiency. For example, most of China’s land is a Se-deficient zone. T.

selenium plant allelopathy ecosystem

1. Selenium Affects Plant-Plant Interactions

Selenium hyperaccumulators can negatively affect the growth and distribution of non-Se accumulators in their vicinity by altering the Se content of the local soil to obtain a large amount of sunlight, water, and other resources for their reproductive survival ^[1]. This phenomenon is one of the Se-polymerizing dynamics of Se hyperaccumulators. The Se content in A. bisulcatus root domain soil can reach 71–103 mg·kg⁻¹ DW, which is three–five times higher than that in the inter-root environment of non-Se accumulators ^[2]. Se-sensitive A. thaliana grown in the root domain soil of Se hyperaccumulators had a significantly lower germination rate and dry weight compared with those grown in the root domain soil of non-Se accumulators ^[2]. These findings suggest that plants may use their Se-polymerizing ability to improve their ecological advantage.

Mehdawi et al. ^[3] indicated that Se hyperaccumulators promote the growth of nearby Se-tolerant plants. The Se content of soil around the Se hyperaccumulator S. pinnata was approximately 7–13 times higher than that in the soil around non-Se accumulators. The Se content in the leaves of Artemisia ludoviciana and Symphyotrichum ericoides growing naturally near the Se hyperaccumulator S. pinnata in Colorado, USA was 10–20 times that when they are at a distance from Se hyperaccumulators. In addition, the plant heigh increased by two–three times, and statistically the plants had more leaves when they were grown near Se hyperaccumulators. This finding indicates that Se hyperaccumulators significantly promote the growth of A. ludoviciana and S. ericoides in their vicinity ^[3]. The above study showed that Se hyperaccumulators have more pronounced ecological effects compared with their surrounding Se accumulators and non-Se accumulators.

Plants release organic Se into the soil in the form of apoplast and root secretions, which increase the organic Se content into the soil and are readily absorbed and utilized by plants ^[4]. The Se content and organic Se content in soil are proportional to the Se content in the surrounding plants ^[3]. Reynolds et al. studied three different Se-enriched areas in the United States and found high Se content in the soil in the Pine Ridge Natural Area, Cathy Fromme Prairie Natural Area, and Coyote Ridge Natural Area close by to the Se hyperaccumulators S. pinnata and A. bisulcatus ^[5]. In addition, the Se content decreased rapidly beyond 50 cm of their roots. This finding was consistent with the canopy width of hyperaccumulators and indicated that hyperaccumulator plants have a concentration effect in terms of Se, that is, the high Se content in their tissues has a significant effect on their adjacent plant communities ^[5]. The high Se content of the soil under the plant canopy may be caused by the high Se content in the fallen leaves; root secretions may also play a role. In addition, hyperaccumulators can transfer Se from underground to surface soils through the root system or enrich Se to the central soil, forming a relatively high Se “enrichment zone” ^[3]. By comparing the Se content of soil within 3 m around 22 Se hyperaccumulators and 22 non-hyperaccumulators at the Pine Ridge Natural Area, the average Se content around hyperaccumulators was two times higher than that around non-hyperaccumulators. This result suggests that the Se content of soil is related to Se hyperaccumulators ^[5]. A 5% increase in bare land area, 7% increase in plant species richness, and 7% decrease in plant canopy cover were observed in the area within 1.5 m of Se hyperaccumulators compared with that of non-Se hyperaccumulators ^[5].

A possible cause for this is that the excessive Se content in the soil near hyperaccumulators restricts the growth of the surrounding plants and to some extent inhibits the growth of some plants that should occupy most ecological niches, allowing less competitive species to have access to resources, such as sunlight and water, for growth and reproduction. As a result, the characteristics of the surface vegetation are altered ^[6]^[7]^[8]. In a word, Se hyperaccumulators can collect, transform, and release Se in the ecological environment by an absorption and transformation progress. In turn, the above-mentioned process changes the Se speciation and distribution in soil, thus regulating the vegetation characteristics in the surrounding environment of Se hyperaccumulators.

2. Selenium Affects Plant-Animal Interactions

Selenium in soil is absorbed, transformed, and metabolized by plants to produce other Se-containing compounds, some of which are volatile, such as DMSe and DMDSe. These volatile selenides often have special odors that have a deterrent effect on herbivores, and some can even be detected by human olfaction ^[9]. Quinn et al. ^[10] found that Se in plant tissues and volatile Se compounds can reduce the foraging behavior of herbivores. In a field setting, Cynomys ludovicianus groundhogs tend to feed on plants with low Se content within the same plant species; this behavior was consistent with findings in relation to non-Se accumulators, such as Brassica juncea, versus Se hyperaccumulators, such as S. pinnata. B. juncea reduced the chance of feeding by C. ludovicianus groundhogs when the Se content reached 38 mg·kg⁻¹ DW or above ^[10]. C. ludovicianus and some Orthoptera may rely on their olfactory perception of volatile Se compounds ^[10]^[11].

High levels of selenide can be a deterrent and toxic to animals ^[11]. Aphids (Myzus persicae) avoid eating B. juncea leaves with Se levels of up to 10 mg·kg⁻¹ DW. Feeding aphids using Indian mustard leaves with a Se content of 1.5 mg·kg⁻¹ DW caused Se poisoning and death ^[12]. When the Se concentration exceeded 0.4 mg·kg⁻¹, the pupation rate of honeybee (Apis mellifera) larvae was significantly reduced, indicating that high Se concentrations have a negative effect on A. mellifera larvae ^[13]. The consumption of pollen and nectar with high Se contents reduced the pupation rate of A. mellifera larvae and impaired the normal physiological functions of honeybees. Long-term memory tests on honeybees revealed that feeding with sugar water containing 3 μL of sodium selenate at a concentration of 6 mg·L⁻¹ decreased the memory of bees, indicating that exposure to excess Se causes bees to exhibit learning and memory deficits. This effect may reduce the ability of worker bees to gather resources and care for the colony ^[14]. When honeybees (Apis mellifera L.) were fed different concentrations of selenate and selenite (60–600 mg·L⁻¹), they exhibited different degrees of oxidative stress ^[15]. Excess Se is harmful to animals, but Se deficiency decreases the ability of animals to synthesize antioxidant enzymes (such as SOD), which leads to enhanced lipid peroxidation activity and increased free radical levels and malondialdehyde content. Moderate amounts of supplemental Se can improve these symptoms ^[16]. The dietary inclusion of 0.32–0.36 mg·kg⁻¹ sodium selenite was effective in enhancing the antioxidant capacity of Italian honeybee larvae and improving their pre-pupal weight and pupation rate ^[13]. These results indicate that excessive Se may damage the normal physiological function of animals.

Long-term natural selection has made some animals tolerant to Se, and this relative Se tolerance may help plants gain an ecological advantage in environments with high Se contents. The Se content accumulated in the flowers of the Se hyperaccumulator S. pinnata can reach 2323 mg·kg⁻¹ DW, and the nectar can contain 244 mg·kg⁻¹ FW ^[8]. The Se in S. pinnata pollen does not hinder the pollination behavior of honeybees, and 0.4–1.0 mg·kg⁻¹ FW of Se was detected in adult bees that fed on these pollens ^[8]. To investigate whether high levels of Se affect bees’ pollen feeding on plants, Colin et al. placed high and low Se plants (treated with 80 μmoL and 0 μmoL Se, respectively) at 10 m from the colony. During the experiment, the positions of the plants were exchanged once ^[8]. The results showed that the bees did not avoid the pollen of plants with high Se contents, and no significant difference in the number of foraging sessions was observed between the high- and low Se pollens ^[8]. A similar finding was obtained in another study where the number of pollen pickings by bees did not decrease or increase after the Se treatment of radish (Raphanus sativus) ^[17].

Freeman et al. ^[18] found that a variety of Plutella xylostella could survive normally on plants with high Se contents. The Se content in larvae and adults was approximately 200 mg·kg ⁻¹ DW, which is 10 times higher than that in normal P. xylostella. Comparative studies between Se-tolerant and Se-sensitive P. xylostella revealed that the former had no significant preference for high and low Se plants and the latter laid significantly fewer eggs on high Se plants than on low Se plants. The natural screening of Se-tolerant moths on high-Se plants, especially Se hyperaccumulators, possibly allowed this variant to tolerate Se at higher levels compared with other Se-sensitive moths, thus facilitating competition between Se-tolerant moths and other herbivores. The study also found that Se was mainly distributed in the abdomen of wild-living Se-resistant P. xylostella, and the Se content of parasitoids was also high, with the high Se content in their bodies likely protecting them from predators. Selenium-tolerant P. xylostella isolate Se in their hindgut or in deposits on the outside of their abdomen, suggesting that they may use the accumulated Se to reduce the risk of predation ^[18]^[19]. The above studies showed that pollinators did not take the initiative to avoid Se-containing plants, implying that high Se contents in plants may prompt pollinators to evolve Se tolerance. The research on the regulating function of Se between plants and pollinators is still insufficient, but the question of how insects evolve Se tolerance under the pressure of environmental selection with high Se contents is an important scientific issue that deserves our continuous attention.

3. Selenium Affects Plant-Microbe Interactions

Plant growth and development are closely related to the activity of microbes, which are distributed within the plant, on the surface, and between the roots. The relationship between microorganisms and plants may be mutually beneficial or neutral or may lead to diseases. Plants provide microorganisms with the nutrients required for their life activities, and microorganisms improve plant resistance and facilitate water and nutrient uptake by plants ^[20]. Microorganisms can assist plants in the uptake of Se from the environment. Inoculation with Funneliformis mosseae and Glomus versiform for eight weeks significantly promoted the uptake of selenate and selenite by the root systems of wheat (Triticum aestivum) seedlings which were planted in the sterilized soil sand mixture ^[21]. Indian mustard inoculated with rhizosphere bacteria exhibited an approximately fivefold increase in root Se content compared with the commonly cultivated plant ^[22]. Some microorganisms can influence the forms of Se in plants. Some endophytic bacteria isolated from plants can reduce sodium selenite to elemental Se in media containing sodium selenite ^[23]. The elemental Se in the Se hyperaccumulators S. pinnata and A. bisulcatus accounts for 35% of their total Se content ^[19]. However, an experiment involving growing sterilized seeds of these two plants in a greenhouse revealed that these two Se hyperaccumulators mainly accumulated organic Se, such as seleno amino acids, and did not accumulate elemental Se in their bodies ^[24]. Elemental Se is not soluble for plant cells and is excreted by the plant, so these endophytic bacteria can help the plant to reduce Se accumulation and enhance the host plant’s tolerance to Se.

Selenium in plants has a suppressive effect on some pathogenic microorganisms, and Se hyperaccumulators can enhance the disease resistance of plants. For example, Hanson et al. reported improved disease resistance in mustard seedlings treated with Se ^[25]. After sterile mustard seedlings grown on agar medium with or without Se were immersed in Fusarium sp. spore suspension, the Se-treated mustard seedlings (with a Se content of approximately 800 mg·kg⁻¹ DW) and the control were infected by Fusarium sp. The fresh weight of the mustard seedlings without Se decreased by 14% after seven days, and that of mustard seedlings with Se increased by 1%. This result indicates that a certain level of Se in mustard seedlings can reduce the damage caused by the pathogenic fusarium on mustard. Therefore, enrichment with certain concentrations of Se enhances plants’ resistance to pathogenic bacterial infestation, and this effect may be one of the intrinsic motivations for Se enrichment in plants.

Plant root microorganisms isolated from soils with high Se contents are more tolerant to Se than those from low Se areas. An analysis of the Se tolerance of plant root microorganisms collected from four Se-enriched and one non-Se-enriched regions in Colorado and Wyoming revealed that plant root microorganisms from Se-enriched regions were not sensitive to 10 mg·L⁻¹ sodium selenates in the medium. Meanwhile, the microorganisms from non-Se-enriched regions were highly sensitive to the same concentration of Se ^[26]. The greater Se tolerance of plant root microorganisms from Se-enriched areas suggests that they may have an adaptive advantage to Se-enriched areas. Given that the Se content in the roots of Se hyperaccumulators can reach 100 times that of non-Se accumulators, microbial populations growing in their vicinity face great evolutionary selection pressure ^[27]. In summary, microorganisms favor enhanced Se tolerance in host plants and resistance to environmental stress, and host plants promote Se tolerance in inter-rooted microorganisms to some extent. Plants release organic Se into the soil, the absorption and transformation of organic and inorganic Se by microorganisms is an important intermediary in the Se cycle. Therefore, the coevolution mechanism of plants and microorganisms in high Se content environments is an interesting scientific topic.

References

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1. Selenium Affects Plant-Plant Interactions

2. Selenium Affects Plant-Animal Interactions

3. Selenium Affects Plant-Microbe Interactions

References